Coordination through inhibition: control of stabilizing and updating circuits in spatial orientation working memory

Abstract

15Spatial orientation plays a crucial role in animal navigation. Recent studies of tethered 16Drosophila melanogaster (fruit fly) in a virtual reality setting showed that the 17 orientation is encoded in the form of an activity bump, i.e. localized neural activity, in 18 the torus-shaped ellipsoid body (EB). Moreover, a fly can maintain working memory of 19 its orientation with a stable and persistent activity bump in the absence of any visual 20 cue, and update the memory in accordance with changes of the body orientation by 21shifting the location of the bump. Although the neural circuit that is responsible for 22shifting the bump has been extensively studied lately, how the nervous system shifts 23 the bump while maintains its stability and persistence is poorly understood. We 24 investigated this question using free moving fruit flies in a spatial orientation memory 25 task, and manipulated two EB subsystems, the P circuit, which has been suggested 26 for the stabilization function, and the C circuit, which has been suggested for the 27 updating function but was largely overlooked. We discovered that overactivating either 28 circuit produced distinct behavioral deficits, confirming that the two circuits play 29 important but different roles in the orientation working memory. Furthermore, 30 suppressing either circuit disrupted the memory, suggesting that the C or P circuit 31 alone is not sufficient to maintain the orientation working memory. We reproduced the 32 observations with a spiking neural network model of EB and demonstrated that spatial 33 orientation working memory requires coordinated activation of the stabilizing and 34 updating neural processes in different movement modes. 35 36 Keywords 37 Central complex, ellipsoid body, spatial orientation memory, working memory, Buridan's 38 paradigm, Drosophila melanogaster 39 40 Introduction 41Maintaining spatial orientation is a crucial cognitive capability required for animal 42 navigation [1,2], and understanding the detailed neural mechanisms of spatial orientation 43 is of great interest to researchers in the fields of neurobiology [3][4][5] or neuromorphic 44 engineering [6][7][8]. In recent years, significant progress has been made in identifying the 45 neural circuits that support spatial orientation [9] in the central complex of Drosophila 46 melanogaster [10,11]. The central complex has long been associated with short-term 47Recently, a model of the EB-PB circuits proposed in Su et al., (2017) was built strictly 64 based on connectomic data and provided a detailed picture of the neural circuit 65 interactions underlying spatial orientation and its working memory [15]. The model 66suggests the involvement of two sets of coupled circuits that connect the EB and PB. One 67 set that consists of EIP (or E-PG) and PEI neurons forms symmetric recurrent connections, 68 and the other set that consists of EIP and PEN (or P-EN) forms asymmetric recurrent 69 4 connections [20,21]. The symmetric circuit, named the C circuit in this paper, forms an 70 attract...

Characterizing approach behavior of Drosophila melanogaster in Buridan’s paradigm

“…They spent more time moving along the edge as evident by the denser distribution of traces in the outer rim area than in the inner circle. This observation is consistent with the common notion of the open-region avoidance behavior of fruit flies, in particular for those without functioning wings [ 9 , 14 ]. This result indicated that the arena did provide a homogeneous illuminating environment without any cue that can elicit directional bias ( Fig 1E–1G ).…”

“…It is interesting to note that, fruit flies with different genetic backgrounds may perform differently in Buridan’s paradigm. For example, although the white-eyed w 1118 flies are known to have poor vision, in another ongoing study we discovered that this types of flies actually perform decently in an arena that used dimmer green LEDs as the light source [ 14 ]. Therefore, the optimal experiment setup may well depend on the strain of the flies and is worth a systematic study in the future.…”

“…Moreover, several recent studies on spatial orientation memory of fruit flies [2,3,18,19] have utilize the approach or fixation behavior as the behavioral measure, and the central complex [20] has been found to be strongly associated with the spatial orientation memory. Therefore, the present behavior level study may provide detailed metrics that helps with extending the computational models of the central complex [14,19,[21][22][23][24][25][26] and linking the neural circuit level mechanisms with the behavior.…”

The neuroanatomical ultrastructure and function of a biological ring attractor

“…Overall, our results confirm that the Drosophila heading direction network contains the core components of a ring attractor while also revealing unpredicted structural features that might enable the heading system to accurately track the animal's heading with a small number of neurons. Importantly, however, these and other models of attractor networks in the fly have assumed the circuit's connectivity based on relatively indirect evidence (Cope et al, 2017;Han et al, 2019;Kakaria and de Bivort, 2017;Kim et al, 2017;Su et al, 2017;Turner-Evans et al, 2017). For example, the location of pre-and post-synaptic arbors has been inferred from whether neural processes visible in light-microscopic images seem spine-or bouton-like in specific substructures (Hanesch et al, 1989;Lin et al, 2013;Wolff et al, 2015).…”